Download and siphonaria concinna

J. Moll Stud. (1997), 63,121-130
© The Malacological Society of London 1997
TEMPORAL VARIATION IN FORAGING BEHAVIOUR OF
PATELLA GRANULARIS (PATELLOGASTROPODA) AND
SIPHONARIA CONCINNA (BASOMMATOPHORA) ON A
SOUTH AFRICAN SHORE
D.R. GRAY and A.N. HODGSON
Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown, 6140, South Africa
(Received 18 May 1996, accepted 2 September 1996)
ABSTRACT
the structuring of intertidal communities
through their grazing activities and corresForaging activity of two mid- to low- shore species of
ponding dislodgment of other settling species
limpet, Patella granulans (Prosobranchia) and
Siphonaria concinna (Pulmonata) from an exposed whilst also adding a valuable energy source to
the community in the form of mucus (Branch,
shore on the Eastern Cape coast of South Africa was
1985; Branch & Barkai, 1988). The importance
monitored. In both species, activity was compared
of limpets in the ecology of rocky shores has
during spring and neap tides and, in P. granulans
between summer and winter. Rhythms of activity of
prompted numerous studies on their activity
the two species were similar, with foraging excurand foraging behaviour, although the majority
sions being mainly associated with nocturnal low tide
of such studies have centred on northern
times, although some P. granularis foraged during
hemisphere species (see Hawkins & Hartnoll,
daytime low tides. It is suggested that foraging
1983; Little, 1989 for reviews of literature).
excursions in P. granularis are triggered by wave
Many species of limpet home to a fixed scar
action. Both species foraged further on spring tides
(Underwood, 1979; Branch, 1981) when not
than on neap tides and this is suggested to be a result
of the limited time limpets have to forage. P. granu- active. Their activity patterns are also believed
laris was also found to forage further during summer to be governed by endogenous rhythms
when compared to winter and the possibility that
(Funke, 1968) and this has recently been
seasonal micro-algal productivity influences foraging
proven to be the case for Patella vulgata (Delia
distances in limpets is discussed.
Santina & Naylor, 1993). A limpet's foraging
The foraging activity of both species could be
movements are therefore limited to an area
divided into 3 distinct phases, a relatively rapid outthat allows a return trip within one activity
ward phase, a much slower foraging phase and a period (Little, Williams, Morritt, Perrins &
rapid homeward phase. Whether or not these
Stirling, 1988). This activity period may occur
limpets graze throughout an excursion is not known.
whilst the limpets are emersed, submersed or
S. concinna was found to home to a fixed scar,
when being splashed by rising and falling tides,
although during the experiment some scar-swapping
occurred. P. granularis did not home to a fixed scar depending on the species (Branch, 1981).
but possessed a 'home range' (approx. 5 cm2) to
Patella vulgata for example has been shown to
which it returned after each excursion.
be active under all of these states of the tide at
Patella granularis was found to move randomly different localities around the British Isles
during foraging, whilst S. concinna foraged in a non- (Hawkins & Hartnoll, 1982; Hartnoll, 1986;
random direction .which took individuals upshore.
Gray & Naylor, 1996).
No tidal-influence is thought to be present in this
Much of the work on limpet activity has
case and the possibility of a learning component in
involved limpet populations from sheltered
the foraging behaviour of certain limpet species in
relation to the return to optimal feeding patches is
shores, such as Menai Bridge, U.K. (Chelazzi,
discussed.
Santini, Parpagnoli & Delia Santina, 1994) and
Port Erin, Isle of Man (Hartnoll & Wright,
1977; Hawkins & Hartnoll, 1982). Lough
Hyne, southern Ireland, which has been the
INTRODUCTION
location of many limpet behavioral studies
Prosobranch and pulmonate limpets are often (Little & Stirling, 1985; Little et al., 1988;
the most dominant organisms on exposed Little, Morritt, Paterson, Stirling & Williams,
1990) not only is a sheltered site, but also
rocky shores and therefore play a major role in
122
D.R. GRAY & A.N. HODGSON
exhibits an abnormal tidal regime (Little,
Partridge & Teagle, 1991). A study to compare
limpet activity inside and outside of the Lough
(Little el al., 1991) found that foraging
intensity differed significantly.
The rocky shores of South Africa are, on the
whole, a highly exposed and extreme environment with a particularly diverse limpet fauna,
with some species occurring in large densities
(Branch, 1971). Except for the work of Branch
& Cherry (1985) on the pulmonate limpet
Siphonaria capensis, very few quantitative
studies have been carried out on the foraging
behaviour of South African limpets, although
results from numerous qualitative observations
(i.e. documenting when animals are active in
relation to the tide) of west coast limpets and
those inhabiting False Bay (Cape Town) have
been published (Branch, 1971; Branch, 1981).
These observations were made during only
one season and so do not reveal anything
about long term (inter-seasonal) or short term
(e.g. effects of spring or neap tides) variation
in foraging behaviour.
The aim of this work was to examine
and quantify the foraging activity of two midto low-shore species, Siphonaria concinna
Sowerby, 1824 (Pulmonata) and Patella granularis Linnaeus, 1758 (Patellogastropoda) from
an exposed shore on the Eastern Cape coast of
South Africa. In both species, activity was
compared during spring and neap tides and, in
P. granularis, in both summer and winter.
MATERIALS & METHODS
Limpets were studied at Cannon Rocks in the Eastern Cape (33° 44' S; 26° 35' E), an exposed boulder
beach composed of quartzitic sandstone and experiencing semi-diurnal tides. The tidal range at Cannon
Rocks is 1.9 m above Chart Datum on mean spring
tides, and 0.9 m on mean neap tides with highest
spring tides phased around 0400 and 1600 hrs (S.A.
Navy tide tables, 1995).
During day-time low tides, Siphonaria concinna
form clusters of between 3 and 35 individuals,
aggregating inCTevicesand/or indentations on the
surfaces of boulders. The group chosen for this study
(mean shell length = 17.96 mm ± 1.9 mm) was
resident on a large (about 1 m2) horizontal boulder
which enabled easy identification of individuals and
accurate measurements. The Patella granularis
chosen were located on a vertical surface of a west
facing rock (mean shell length = 19.87 mm ± 2.4
mm). Neither set of limpets had any protection from
wave action and both occurred at a similar tidal level
within the lower balanoid zone (1.1 ± 0.2 m above
Chart Datum).
Twelve hours prior to recordings, 20 limpets of
each species were marked with small plastic numbers
(Dymo tape) attached to the shell with epoxy resin
(Cook, Bamford, Freeman & Teideman, 1969) after
removing all encrusting material from the surface of
the shell and blotting off excess water. In order to
determine whether limpets had a consistent orientation on a home scar, individuals were marked with a
line of cellulose paint from the apex to the margin of
the shell (Little & Stirling, 1985). The line was
extended on to the adjacent rock face so that when
the limpet was 'home', the line was continuous. The
limpet's number was painted on the rock next to
each limpet. The position of any individual at any
given time was determined by triangulation (Cook et
al., 1969). Three crosses equidistant from each other
(50 cm for S. concinna, 100 cm for P. granularis)
were painted on the rock. Using these crosses as
reference points, the path of each limpet could be
plotted to an accuracy of ± 4.6 mm.
Activity (= limpet movement) of S. concinna was
recorded on a spring full moon, two spring new
moons and a neap quarter moon during winter
(Table 1). For P. granularis activity was recorded on
spring and neap tides in both Summer and Winter.
Previous observations on short term behavioural
patterns of Helcion pectunculus within tides and
seasons have shown very little variability (Gray &
Hodgson, unpublished) and so replications were not
carried out during this study. Measurements were
carried out at hourly intervals from "when the limpets
were uncovered by the tide to re-submergence.
Measurements were not taken during high tide due
to intense wave activity in the intertidal zone making
observations impossible. It was, however, assumed
that the limpets remained inactive during immersion
due to the fact that they returned to a home scar or
site before being covered by water. It has also previously been observed that P. granularis remain inactive during high tide (Thorpe, 1962) as do many
species of Siphonaria (Branch, 1981; Branch &
Table 1. Dates of observation periods for both
Siphonaria concinna and Patella granularis
showing the phase of the tide and the season.
Tidal phase
Siphonaria concinna
26.04.94
Spring Full Moon
10.05.94
Spring New Moon
17.05.94
Neap Quarter Moon
11.08.94
Spring New Moon
Patella granularis
14.03.95
Spring Full Moon
25.03.95
Neap Quarter Moon
02.03.05
Spring New Moon
14.07.95
Spring Full Moon
20.07.95
Neap Quarter Moon
26.07.95
Spring New Moon
Season
Winter
Winter
Winter
Winter
Summer
Summer
Summer
Winter
Winter
Winter
FORAGING BEHAVIOUR OF P. GRANULARIS & 5. CONCINNA
Cherry, 1985) presumably due to their extremely low
tenacity.
Limpets were recorded as 'at home' when they
were on their home scar and as 'active' when away
from their home scar. At night, observations
were made using only red light since previous studies
have shown that white light causes limpets to clamp
down and cease foraging (Cook et al., 1969; Little &
Stirling, 1985; Gray & Naylor, 19%).
During the observations on P. granularis, physical
variables were measured hourly whilst limpets were
emersed. Measurements included rock and air
temperature (Hanna instruments HI 9040 microcomputer
thermometer),
relative
humidity
(Hygrocheck relative humidity probe) and light
intensity in n E m ' V (Integrating Quantum/
radiometer/photometer, model LI-188B by Licor
inc.). Weather conditions were noted on an hourly
basis.
A 'foraging angle' was calculated for each
excursion for both S. concinna and P. granularis by
plotting a line through the home scar and the
furthest point reached by the limpet during that
123
excursion and measuring the angle in a clock-wise
direction from magnetic North (5. concinna) and
the vertical (P. granularis). The mean vector (r) of
foraging directions of the two samples, irrespective
of the maximum distance travelled, were calculated
(Mardia, 1972; Batschelet, 1981).
RESULTS
Activity Rhythms
In both species, limpets foraged primarily during low tide which occurred at night or around
dusk and dawn (Figs 1, 2 & 3). P. granularis
was, however, found to forage during day time
low tides in summer, although such movement
mainly took place in the shade (248-890
H-Etrr^"1). Foraging in P. granularis began as
the limpets were being washed by waves on
the ebbing tide. Individuals were still active,
although almost home, as they were covered
100 -
12
14
16
18 20
22 24
Time in hours
8
10 12
12
14
16
18 20
22 24
2
4
8
10 12
Time in hours
Figure L The percentage of Patella granularis active Figure 2. The percentage of Patella granularis active
recorded every hour for 24 hrs during 3 summer
recorded every hour for 24 hrs during 3 winter
observation periods a) 2.3.95, b) 253.95 & c) 17.3.95.
observation periods a) 26.7.95, b) 20.7.95 & c)
Arrows indicate times of low tide. Shaded bar
14.7.95. Arrows indicate times of low tide. Shaded
indicates period of darkness.
bar indicates period of darkness.
124
D.R. GRAY & A.N. HODGSON
New Mooo
t • T • t * t
12
' f
•
(b)
Neap Quarter Moon
(C)
Spring Full Moon
14
16
18
20
22
24
2
4
8
10 12
Time in hours
Figure 3. The percentage of Siphonaria concinna
active recorded every hour for 24 hrs during 3 winter
observation periods a) 11.8.94, b) 17.5.94, c) 26.4.94.
Arrows indicate times of low tide. Shaded bar indicates period of darkness.
with water on the flowing tide. On 5 of the 6
observation periods > 80% of the limpets
were active. The exception was 14/07/95 when
only 50% of the limpets were active. During
the 48 hours prior to this observation period,
24 mm of rainfall was recorded in the Cannon
Rocks area (Met. Office, Port Elizabeth, pers.
comm.).
Siphonaria concinna commenced foraging
soon after emersion and returned to their
home scar prior to immersion on the next
flood tide. On the 10/05/94 (SNM), after it had
rained heavily for the previous 24 h, no movement of the 20 labelled S. concinna was
observed. During the study 100% activity
was never recorded with only 50-72% of
individuals being active at any one timd
Homing behaviour
behaviour (Chelazzi, 1990), as only a small
proportion (10%) of the limpets returned to a
home scar. Limpets did, however, return to the
same area on the rock (approx. 5 cm2) i.e. a
home site. In S. concinna homing was 100%
successful. During the course of the study 16
limpets (80%) exchanged home scars during
the spring-neap-spring cycle (9 during the
spring-neap period, 7 during the neap-spring
period). New positions were considered to be
the home scar for further observations. When
returning to their home scar, S. concinna
rotated their shell until the shell margin fitted
the rock surface exactly. The shell seldom
touched the rock until the correct orientation
was achieved.
Both P. granularis and S. concinna never
returned to their home scar via their outward
path. Trail crossing did occur in both species
but no attempt by individuals to change direction and follow the previous trail was observed
throughout the study.
Distance moved and speed of movement
Both P. granularis and S. concinna travelled
significantly greater distances on spring tides
than on neap tides (Table 2). S. concinna
travelled about twice as far on the spring full
moon compared to either the spring new moon
or the neap quarter moon (p = 0.043;
ANOVA, Table 3).
Patella granularis travelled nearly three
times as far on springs compared to neaps
during the summer period of observation
(Table 4). An analysis was not carried out on
the winter data due to the lack of information
for the neap tide. For P. granularis, limpets
travelled significantly further (up to 5 times as
far; p < 0.001 t-test) in Summer than in Winter
(Table 5).
On all occasions, both P. granularis and S.
concinna moved rapidly away from their home
scar as activity commenced (Table 2). Individuals then slowed down upon reaching a particular area, where they remained for some time
(1-3 hours). Movement back to the home scar
or site was also rapid (figure 4), and after the
correct orientation on the scar was reached (S.
concinna), activity ceased. The speed of movement of P. granularis was significantly slower
in winter (p < 0.05 Mann-Whitney U test).
Orientation offoraging movements
The direction of outward movement of P.
Patella granularis exhibited 'collective' homing granularis did not differ significantly from a
FORAGING BEHAVIOUR OF P. GRANULARIS & S. CONC1NNA
125
Table 2. Mean foraging distances, speed of movement (x ± S.D.) for Siphonaria concinna, Patella
granularis&L Siphonaria capensis during outward (initial 33% of excursion), foraging (second 33% of
excursion) & homeward (final 33% of excursion) phases of foraging excursions (data for S. capensis
taken from Branch & Cherry, 1985).
Mean displacement Outward
Foraging
Homeward
Duration of
± S.D. (cm)
speed (cm/h) speed (cm/h) speed (cm/h) activity (min)
Siphonaria concinna
SFM (26.04.94)
179.0 ± 31.9
79.0 ± 6.2
9.0 + 2.1
53.0 ± 4.5
540
SNM (10.05.94) No movement recorded
NQM (17.05.94)
81.0 ± 29.4
40.0 ± 2.3
5;3 ± 1.6
14.0 ± 2.3
480
31.2 ± 2.9
480
SNM (11.08.94) 106.0 ± 29.1
53.0 ± 4.5
4.6 ± 2.0
Siphonaria capensis
Neap tide
1.1 ± 0.8
Spring tide
6.2 ± 3.9
Patella granu'laris
Summer
10.6 ±3.6
5.7 ±2.2
11.1 ± 4.1
300
SFM (17.03.95)
47.64 ± 4.5
NQM (25.03.95) 13.5 ± 2.3
No distinct outward and homeward sections
SNM (02.03.95) 30.5 ± 5.2
9.6 ± 2.9
6.1 ± 1.8
9.9 ± 3.2
420
Winter
SFM (14.07.95)
7.65 ± 1.89
1.9 ± 0.7
0.9 ± 0.02
4.1 ± 1.2
420
NQM (20.07.95) No measurements taken due to rough sea
1.1 ±0.07
5.1 ± 2.1
240
SNM (26.07.95) 13.75 ±1.63
Table 3. Siphonaria concinna: Results of a multiple range analysis
(Newman-Keuls) between tidal phases i.e. Spring full moon. Neap
quarter moon and Spring new moon.
Spring full moon > Spring new moon = Neap quarter moon
179.0 cm > 106.0 cm
= 81.0 cm
Table 4. Analysis of variance of distances travelled by Patella granularis on the different phases of the tide during the summer period of
observations.
Source of variation
Phase of tide
df
SS
MS
11662.3
5831.1
19.36
0.0001
Results of a multiple range analysis (Newman-Keuls) between phase
of the tides
Spring full moon > Spring new moon = Neap quarter moon
47.65 cm > 30.5 cm
= 13.5 cm
random model (p > 0.05; Rayleigh test).
Siphonaria concinna, however, showed directional movement upshore (Figure 5).
Physical variables
During summer low tides, daytime air and rock
temperatures reached 24.2 ± 2.9 and 27.1 ±
5.2°C respectively (Table 6). The temperature
of the rock surface was generally 1-3°C
warmer than the air temperature during the
day. At night the air and rock temperatures
were similar. Relative humidity of the air was
found to be 20-40% higher at night than
126
D.R. GRAY & AN. HODGSON
Table 5. Analysis of variance of distances
travelled by Patella granularis between seasons.
P
Source of variation
df
MS
F
Season
1
95355
24.361 0.001
Summer > Winter
33.65 cm > 11.2 cm
0
10
20
during the day. In general, temperatures (both
air and rock surface) were lower during the
winter periods of observation than those
recorded during the summer.
30
40
»
60
90
100
% of cicnnkw
DISCUSSION
In the present study, quantitative data on the
foraging activity of two mid-shore South
African limpets was obtained. The intention
was to establish whether these two limpets,
which live at a similar height on the shore in
differing habitats, showed similar behaviour to
each other and to species studied oh more
sheltered shores. The timing of activity of P.
granularis on the east coast of South Africa
agTees with the observations of Branch (1971)
for west coast populations. Movement
Figure 4. Speed of limpets (n = 20) plotted against
percentage of excursion period, a) S. concinna, b)
P. granularis. Solid symbols and continuous line
indicate mean speeds.
Table 6. Air and rock surface temperature ranges (°C) and the
range of relative humidity measurements recorded during activity
observations of Patella granularis during both summer and winter.
P. granularis
Summer
17.03.95 Day
Night
25.03.95 Day
Night
02.03.95 Day
Night
Winter
14.07.95
20.07.95
26.07.95
Day
Night
Day
Night
Day
Night
Range of air
temp. CO
Range of rock
temp. (°C)
Range of rel.
humidity (%)
21.1-27.1
16.0-19.7
18.9-21.9
17.1-18.1
21.2-24.2
19.1-20.5
19.6-32.6
17.2-18.2
20.2-25.6
17.7-17.8
18.3-29.2
19.3-21.0
54.8-70.3
80.4-91.0
68.5-89.6
90.3-93.3
42.8-73.2
92.2-99.7
18.5-20.4
12.2-17.3
16.4-17.6
16.0-17.3
13.2-18.6
13.5-16.8
19.8-26.2
13.1-15.3
18.3-22.6
14.0-14.6
13.4-20.3
14.4-17.4
52.1-56.2
70.8-82.7
29.6-58.6
71.6-86.7
40.6-61.8
69.1-75.3
FORAGING BEHAVIOUR OF P. GRANULARIS & S. CONCINNA
occurred at low tide during both day and night
and appeared to be initiated by spray from
wave action on the ebbing tide. Branch (1971)
also observed that P. granularis in the lower
balanoid zone often lacked a fixed scar and
exhibited random movement, which was also
true for east coast limpets.
Siphonaria concinna exhibited very similar
behaviour to 5. capensis which inhabit exposed
rock surfaces (Branch & Cherry, 1985). Both
species were active at low tide at night, and
both homed to a fixed scar. The ability to
home rigidly seems the norm for most species
of Siphonaria (Branch, 1981; Creese & Underwood, 1982; Garrity, 1984) although 5. virgulata tends to move randomly and usually lacks
a scar (Creese & Underwood, 1982). The activity rhythms of S. concinna may have several
driving factors. Garrity & Levings (1983) suggested that limpets remain inactive at high tide
to avoid marine predators. This is unlikely in
the case of S. concinna, for like many other
siphonariids it secretes mucus containing the
defensive polypropionate Pectinatone (DaviesColeman, pers.comm.). A more plausible
explanation is that by being active at low tide,
5. concinna reduces the chance of being swept
away by wave action as they have a low tenacity (Branch & Marsh, 1978). By contrast, P.
granularis are active under strong wave action
and are known to be highly tenacious (Branch,
1981). Finally, occupying a fixed scar during
the day would reduce desiccation, as has been
shown in other limpets (Verdeber, Cook &
Cook, 1983; Branch & Cherry, 1985; Kunz &
Conner, 1986). Day-time air and rock temperatures were higher than those at night. In addition, the relative humidity at night was always
greater than 70%, thus by being active during
the cooler, more humid conditions, 5. concinna
presumably reduces water loss.
Neither P. granularis or S. concinna
followed outward paths back to their home
scar or site. Cook (1971) showed that the
limpet 5. alternata, can home without using
either distant cues, reverse-displacement or
topographic memory, and indicated that
limpets were capable of following mucus trails.
This does not, however, seem to be the case
for either P. granularis or 5. concinna and
raises the much debated subject of how
limpets home to a fixed scar? Although further
work is required it is possible that individuals
follow previously laid trails, or that different
species of limpet have evolved different
homing methods depending upon their
environment and situation. The fact that the
127
(a)
270°
90°
x - 6.4°
r-= 0.477
n-14
p < 0.05
(b)
270°
90°
x-43.6°
r - 0.894
n-12
p < 0.001
(0
270°
90°
x - 3.44°
r-0.575
n-10
p<0.05
180°
Figure 5. Foraging directions shown by Siphonaria
concinna on a) 26.04.94 SFM, b) 17.05.94 NQM & c)
11.08.94 SNM. Each dot represents one excursion, n
- number of excursions observed and plotted, r - an
estimate of the non-uniformity of the circular distributions given as mean vector lengths by the
Rayleigh test.
128
D.R. GRAY & A.N. HODGSON
limpets cross their own trails without actually amount of food available, thus forcing the
following them may be sufficient to give limpets into a second excursion. Little (1989),
the limpet enough information for correct however, suggests that competition between
limpets of the same species for food would also
orientation.
The foraging activity of P. granularis and S. cause the individuals concerned to forage
concinna could be divided into 3 distinct during the day as well as at night. It has been
phases, a relatively rapid outward phase travel- suggested that barnacles do have an adverse
ling away from the home scar/site, a slower effect on limpets because the rough and irreguforaging phase and a rapid homeward phase. lar topography created by barnacles hinders
Such behaviour has been recorded for Patella limpet foraging behaviour (Lewis & Bowman,
vulgata (Hartnoll & Wright, 1977; Little et al., 1975; Underwood, 1979; Little et al., 1988).
1988; Chelazzi et al., 1994). Although P. Another possibility is that the filter feeding of
vulgata was shown to feed for the entire barnacles reduces available algal spores and
activity cycle, grazing was most intense during sporelings (Branch, 1976). Hawkins and Hartthe middle phase of the cycle (Little & Stirling, noll (1982) have shown that the incidence of
1985; Evans & Williams, 1991). Whether or not foraging in Patella vulgata is proportional to
P. granularis and 5. concinna feed throughout the density of barnacles. Since barnacles
appear to reduce feeding efficiency, increased
their activity cycles is not known.
The activity of 5. capensis during neap and foraging presumably reflects decreased food
spring nocturnal low tides shows that the aver- availability. The presence of barnacles may,
age displacement of limpets from their scars however, result in a damper surface, enabling
and the time spent foraging are both greater limpets to forage without fear of desiccation.
during spring tides than during neap tides This therefore raises the question of whether
(Branch & Cherry, 1985). This also proved to limpets forage at every available opportunity
be the case for 5. concinna. The distance or whether they only forage when they need
travelled by a limpet during an excursion food?
maybe a function of the time exposed to air i.e.
Many species of limpet appear highly opporthe time available for foraging. Siphonariid tunistic. Cellana grata, for example, moves
limpets are limited to foraging whilst exposed, whilst awash, but during typhoons individuals
presumably due to low tenacity, and so move constantly and when artificially sprayed
foraging excursions will be both shorter in time with water, even at low water, will become
and distance on neap tides, thus enabling active (Williams & Morritt, 1995; Williams,
the limpet to return home before being pers. comm.). C. toreuma has been reported to
covered by the incoming tide (Branch & remain active for up to 18 h whilst awash
Cherry, 1985; Branch, 1988). However, the (Hirano, 1979). There is evidence that certain
average displacement of 5. capensis from their limpet species that undergo long feeding
scars is considerably less than that of S. excursions one night are less likely to feed the
concinna (Table 2). A possible reason for following night (Branch & Cherry, 1985) but
this is the large difference in micro-algal more detailed observations are required to
productivity of the east and west coasts of determine whether this is so for all limpets.
Southern Africa (Bustamante, Branch, Different environments may well call for
Eekhout, Robertson, Zoutendyk, Schleyer, different feeding strategies of limpets.
Dye, Hanekom, Keats, Jurd & McQuaid,
Patella granularis showed little seasonal
1995). We tentatively suggest that the west difference in the number of limpets active
coast, with its higher algal productivity, allows during possible activity periods with between
the limpets to forage far shorter distances to 80-100% of the sample being active at any one
obtain enough food for sustenance, whilst 5. time on most occasions. The suppression of
concinna on the east coast has to travel further activity on the evening of the 14/07/95 may be
in order to obtain enough food, although attributed to the heavy rainfall 48 hrs prior to
further work is required to substantiate this.
observation. Fresh water has been shown to
Some P. granularis foraged during daytime suppress limpet activity (Arnold, 1957; Little
low tides as well as at night, c.f. low water P. & Stirling, 1985; Little et al., 1990). This may
vulgata in Lough Hyne (Little et al., 1990; also explain the lack of any movement by S.
Williams & Morritt, 1991), although this only concinna on the 10/05/94 after it had rained
ever took place in the shade (248-890 heavily for the previous 24 hrs.
jiEm~V). It is possible that the presence of
There was a significant difference in the disbarnacles on the rock surface reduces the tance travelled by P. granularis during summer
FORAGING BEHAVIOUR OF P. GRANULARIS & S. CONCINNA
and winter, limpets travelling nearly three
times as far in summer than in winter (Table
1). This could be due to a number of reasons,
firstly epilithic algal production (in the form of
chlorophyll a) per month peaks during the
winter months along the south coast of South
Africa (Bustamante et al., 1995) and so it is
possible that the limpets need not travel as
far to obtain their quota of algae. Cubit
(1984) found this to be true for Collisella
digitalis occurring high up on the shore
(Oregon, U.S.A.). Another possibility is a
reduction in activity due to the cold temperatures in winter compared with those of the
summer period (see Table 3) the limpets
metabolism is much lower and so they do not
need as much food or cannot physically move
as fast due to a reduction in basic bodily
functions (Marshall, 1991).
Patella granularis moved randomly during
foraging, a behaviour previously observed in
lowshore individuals of the species (Branch,
1971). In S. concinna, however, foraging excursions were non-random in direction, with a
mean vector upshore in each case. This vector
actually took the limpets into an area of rock
which had a smooth flat surface compared to
the rough, pitted area within which their home
scars were situated. P. vulgata has been shown
to exhibit directionality during foraging excursions (Little et al., 1988; Gray & Naylor, 1996)
and several other patellids show vertical movements in relation to tidal rise and fall (Hirano,
1979; Williams & Morritt, 1995). However, in
this study the dominant foraging directions
were not in the vertical plane but horizontally
across a rock surface. This rules out the
suggestion of a tidal influence on foraging
direction (Hirano, 1979) in the case of
S. concinna and leans more towards the
possibility of a learning component of foraging
behaviour in relation to the return of optimal
feeding patches (Gray & Naylor, 1996),
although Evans & Williams (1991) have
argued that limpets do not need to maximise
energy given as foraging opportunities are
predictable in certain environments.
ACKNOWLEDGEMENTS
We would like to thank the FRD and Rhodes
University for financial support during this
study, Dr Gray Williams for critically reading
the first draft of the manuscript and L.
Moxham, J. Delport, A. Gordon, K. Buchanan
& P. Joiner for assisting with the field work.
129
REFERENCES
ARNOLD, D.C. 1957. The response of the limpet,
Patella vulgata L., to waters of different salinities.
Journal of the Marine Biological Association of the
U.K., 36:121-128.
BATSCHELET, E. 1981. Circular statistics in biology.
Academic Press, London.
BRANCH, G.M. 1971. The ecology of Patella
Linnaeus from the Cape Peninsula, South Africa.
I. Zonation, movements and feeding. Zoologica
Africana, 6: 1-38.
BRANCH, G.M. 1976. Interspecific competition
experienced by South African Patella species.
Journal of Animal Ecology. 45: 507-529.
BRANCH, G.M. 1981. The biology of limpets: physical
factors, energy flow and ecological interactions.
Oceanography and Marine Biology Annual
Review, 19:235-380.
BRANCH, G.M. 1985. Limpets: their role in littoral
and sublittoral community dynamics. In: The
Ecology of Rocky Coasts (P.G. Moore & R. Seed,
eds), 97-116. Hodder & Stoughton, Kent.
BRANCH, G.M. 1988. Activity rhythms in Siphonaria
theristes. In: Behavioral adaptations to intertidal
life. (G. Chelazzi & M. Vannini, eds), 27^44.
NATO ASI Series, Vol 151, Plenum Press, New
York.
BRANCH, G.M. & BARKAI, A. 1988. Interspecific
behaviour and its reciprocal interaction with
evolution, population dynamics and community
structure. In: Behavioral adaptations to intertidal
life. (G. Chelazzi & M. Vannini, eds), 225-254.
NATO ASI Series, Vol 151, Plenum Press, New
York.
BRANCH, G.M. & MARSH, A.C. 1978. Tenacity and
shell shape in six Patella species: adaptive features.
Journal of Experimental Marine Biology <t
Ecology, 34:111-130.
BRANCH, G.M. &• CHERRY, M.I. 1985. Activity
rhythms of the pulmonate limpet Siphonaria
capensis Q. & G. as an adaptation to osmotic
stress, predation and wave action. Journal of
Experimental Marine Biology <4 Ecology, 87:
153-168.
BUSTAMANTE, R.H., BRANCH, G.M., EEKHOUT, S.,
ROBERTSON, B., ZOUTENDYK, P., SCHLEYER, M.,
DYE, A., HANEKOM, N., KEATS, D., JURD, M.,
MCQUAID, C. 1995. Gradients of intertidal
primary productivity around the coast of South
Africa and their relationships with consumer
biomass. Oecologia, 102:189-201.
CHELAZZI, G. 1990. Eco-ethological aspects of
homing behaviour in molluscs. Ethology, Ecology
and Evolution, 2:11-26.
CHELAZZJ, G., SANTINT, G., PARPAGNOLI, D. &
DELLA SANTINA, P. 1994. Coupling motographic
and sonographic recording to assess foraging
behaviour of Patella vulgata. Journal of Molluscan
Studies, 60: 237-32.
COOK, A., BAMFORD, O.S., FREEMAN, J.D.B. &
TEIDEMAN, D J. 1969. A study of the homing habit
of the limpet. Animal Behaviour, 17: 330-339.
DR. GRAY & AN. HODGSON
130
CREESE, R.G. & UNDERWOOD, A J. 1982. Analysis of
inter- and intra-specific competition amongst
intertidal limpets with different methods of
feeding. Oecologia, S3: 337-346.
CUBIT, J.D. 1984'. Herbivory and the seasonal
abundance of algae on a high intertidal rocky
shore. Ecology, 65:1904-1917.
DELLA
SANTINA,
P.
&
NAYLOR,
E.
1993.
Endogenous rhythms in the homing behaviour of
the limpet Patella vulgata Linnaeus. Journal of
Molluscan Studies, 59: 87-91.
EVANS,
MR.
&
WILLIAMS,
G.A.
1991. Time
partitioning of foraging in the limpet Patella
vulgata. Journal of Animal Ecology, 60: 563-575.
FUNKE, W. 1968. Heimfindevermogen und Ortstreue
bei Patella L. (Gastropoda: Prosobranchia).
Oecologia, 2:19-142.
GARRITY, S.D. 1984. Some adaptations of
gastropods to physical stress on a tropical rocky
shore. Ecology, 65: 559-574.
GARRITY, S.D. & LEVINGS, S.C. 1983. Homing to a
Patella vulgata L. Journal of Experimental Marine
Biology and Ecology, 17: 165-204.
LITTLE, C. 1989. Factors governing patterns of
foraging activity in littoral marine herbivorous
molluscs. Journal of Molluscan Studies, 55: 273284.
LITTLE, C. & STIRLING, P. 1985. Patterns of foraging
activity in the limpet Patella vulgata L.—A Preliminary study. Journal of Experimental Marine
Biology and Ecology, 89: 283-296.
LITTLE, C., WILLIAMS, G.A., MORRITT, D., PERRINS,
J.M. & STIRLING, P. 1988. Foraging behaviour of
Patella vulgata L. in an Irish sea-lough. Journal of
Experimental Marine Biology and Ecology, 120:
1-21.
LITTLE, C, MORRITT, D., PATERSON, D.M.,
STIRLING, P. & WILLIAMS, G.A. 1990. Preliminary
observations on factors affecting foraging activity
in the limpet Patella vulgata. Journal of the
Marine Biological Association of the U.K., 70:
181-195.
scar as a defence against predators in the
pulmonate limpet Siphonaria gigas. Marine
Biology, 72: 319-324.
LITTLE, C , PARTRIDGE, J.C. & TEAGLE, L. 1991.
HAWKINS, SJ. & HARTNOLL, R.G. 1983. Grazing of
VERDERBER, G.W., COOK, S.B. & COOK, C.B. 1983.
Foraging activity of limpets in normal and
abnormal tidal regimes. Journal of the Marine
Biological Association of the U.K., 71: 537-554.
GRAY, D.R. & NAYLOR, E. 1996. Foraging and
homing behaviour of the limpet, Patella vulgata: a MARDIA, K.V. 1972. Statistics of directional data.
geographical comparison. Journal of Molluscan
Academic Press, London.
Studies, 62:121-124.
MARSHALL, DJ. 1991. Environmental physiology of
the intertidal limpets Patella (Prosobranchia) and
HARTNOLL, R.G. 1986. The monitoring of limpet
Siphonaria (Pulmonata), with particular reference
movement: a review. Progress in Underwater
to their metabolic adaptations. PhD Thesis,
Science, 11: 137-146.
Rhodes University, South Africa.
HARTNOLL, R.G. & WRIGHT, J.R. 1977. Foraging
movements and homing in the limpet Patella
SOUTH AFRICAN NAVY TIDE TABLES. The Hydrovulgata L. Animal Behaviour, 25: 806-810.
grapher. S. A. Navy, Tokai.
THORPE, W.H. 1962. Learning and instinct in
HAWKINS, SJ. & HARTNOLL, R.G. 1982. The influAnimals. Methuen, London.
ence of barnacle cover on the numbers, growth
and behaviour of Patella vulgata on a vertical pier. UNDERWOOD, AJ. 1979. The ecology of intertidal
Journal of the Marine Biological Association of the
gastropods. Advances in Marine Biology, 16:
U.K., 62: 855-867.
111-210.
intertidal algae by marine invertebrates. Oceanography and Marine Biology Annual Review, 21:
195-282.
HIRANO, Y. 1979. Studies on activity pattern of the
Patellid limpet Cellana toreuma (Reeve). Journal
of Experimental Marine Biology and Ecology, 40:
137-148.
KUNZ, C. & CONNER, V.M. 1986. Roles of the home
The role of the home scar in reducing water
loss during aerial exposure of the pulmonate
limpet Siphonaria altemata (Say). Veliger, 25:
235-243.
WILLIAMS, G.A. & MORRITT, D. 1991. Patterns of
foraging in Patella vulgata (L.). In: The Ecology of
Lough Hyne. (A. Myers, C. Little, M. Costello &
J. Partridge, eds), 61-69. Royal Irish Academy.
scar of Collisella scabra (Gould). Veliger, 29: WILLIAMS, G.A. & MORRITT, D. 1995. Habitat parti25-30.
tioning and thermal tolerance in a tropical limpet,
Cellana grata. Marine Ecology Progress Series,
LEWIS, J.R. & BOWMAN, R.S. 1975. Local habitat124: 89-103.
induced variations in the population dynamics of